The ecological and evolutionary significance of sex-reversal in Australian lizards

Abstract

Conventional wisdom holds that sex determination is categorised into mutually exclusive systems: genetic sex determination (GSD) where sex is determined by a sex determining gene or genes located on the sex chromosomes or environmental sex-determination (ESD) where there are no sex chromosomes, and where sex is likely determined entirely by environmental factors at a critical stage of embryonic development. Reptiles exhibit a wide variety of sex determining mechanisms, which include multiple chromosomal forms (XX/XY & ZZ/ZW), a form of environmental sex determination (temperature-dependent sex determination [TSD]), and some in which GSD and TSD interact to determine sex. This GSD and TSD interaction is known as sex-reversal, where an environmental cue (e.g., temperature) can interact with sex chromosomes to reverse the sex. In these situations, sex-reversed individuals will exhibit a dis-concordance in their genotype (e.g., XX male) compared to the concordant phenotype (e.g., XY male/ non sex-reversed). Although reptiles have transitioned between GSD and TSD many times, the ecological processes that drive these transitions have remained unknown. Using a combination of laboratory and field experiments, my research focused on a detailed examination of the ecological and evolutionary significance of sex-reversal in lizards. I first propose a framework to test how fitness-related traits vary across sex classes for systems with sex-reversal and how these traits may influence frequencies of each sex within a population over time. Within this framework, I focus on 1) quantifying the performance of sex-reversed individuals in fitness-related traits and how this relates to phenotypic and chromosomal sex; 2) determining if these patterns persist in wild populations; 3) identifying the frequency of sex-reversal within a population and how this changes over time across populations; and 4) examining gene flow or dispersal across populations and how this varies across sex.
In the laboratory, I measured three traits related to fitness (metabolism, growth rate, and survival) in hatchling lizards of two species with different patterns of temperature-induced sex-reversal, Bassiana duperreyi and Pogona vitticeps. There were no differences in survivorship across sex for either species. Metabolic and growth rates for sex-reversed individuals were more reflective of their reproductive phenotype rather than their chromosomal complement. This evidence indicates these traits are not linked to genes on the sex chromosomes, but rather these processes may arise due to gonadal effects (i.e. sex hormones or other modifiers that orchestrate sex-biased gene expression) during embryonic development. Overall, I find weak evidence that sex-reversal conveys a fitness advantage in either species, but energetic processes may still constrain the distribution of sex-reversal in nature. However, I do not rule out the possibility of sex differences emerging through ontogeny. This is the first study to explore the metabolic consequences of sex-reversal in lizards or any other vertebrate.
I then tested components of the Like Phenotype/Genotype Framework using field and laboratory experiments on adult P. vitticeps. Here I combined genotype-by-sequencing, identification of phenotypic and chromosomal sex, exhaustive field surveys, and radio telemetry to examine levels of genetic structure, rates of sex-reversal, movement, space use, and survival. I found low levels of population structure (high degree of individual dispersal), but no increase in proportions of sex-reversal in samples taken during 16 years in an area where sex-reversal was spatially clustered in the southeastern part of the species range. In a population I studied intensively for 16 months, I documented moderate levels of sex-reversal within a population (25%). Although there were similarities in survival and vagility (movement and home range) between sex-reversed and concordant females (ZWf), ZWf individuals were more fecund. I provide further support for the Like Phenotype Hypothesis using adult P. vitticeps in the laboratory, where I found that the thermal preference for sex-reversed and concordant females was more similar in comparison to male counterparts.
Finally, I tested fundamental questions regarding thermal ecology in ectotherms by applying new telemetry technologies. I used a combination of accelerometer and thermal data to quantify the thermoregulation and performance of P. vitticeps in situ over one year. I provide a new approach using accelerometers to construct field thermal performance curves (TPC) and develop workflows to extract TPC parameters across four seasons. These data were used to test predictions of the cost-benefit model of thermoregulation between sex. I then assessed the costs of thermoregulation, determining how thermal and performance indices of individuals relate to survivorship during the reproductive season when this species is most active and experiences its highest predation pressures. Across multiple seasons I found that P. vitticeps followed the general predictions from the cost-benefit model of thermoregulation. Specifically, thermoregulation occurred when the environmental costs were low (when temperatures were within their preferred body temperature range) and when the environmental costs were high (when temperatures were outside their preferred body temperature range), behaviours became constrained, and individuals conformed to the environment. However, during the reproductive season (spring), I found that there were trade-offs of thermoregulation that differed markedly by sex. These differences resulted in a decrease in survivorship which corresponded with the poor ability of female lizards to thermoregulate. These data indicate that sex-specific measures during reproductive seasons would improve the accuracy of testing trade-offs of the cost-benefit model of ectothermic thermoregulation in the wild.
In both laboratory and field experiments, I found strong evidence for the Like Phenotype Hypothesis in metabolism, thermal ecology, fecundity, behaviours, and survivorship for temperature induced sex-reversal in reptiles. These similarities between sex-reversed and concordant phenotypic sex indicate that there are no clear advantages of sex-reversed counterparts over the concordant phenotypic sex that would create an imbalance of frequencies of homogametic chromosome (XX or ZZ). I argue that in these systems, at their current state, the lack of differences in fitness-related traits between sex-reversed and their concordant phenotypes would not drive the evolution of a new temperature-based sex determining system.

Date of Award	2022
Original language	English
Supervisor	Arthur GEORGES (Supervisor), Stephen SARRE (Supervisor), Lisa SCHWANZ (Supervisor) & John Roe (Supervisor)